The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks

In the paper

“Unfortunately, reef corals are losing this critical reproductive synchrony, likely due to anthropogenic impact [22,23].”

What the sources say

• Not checked yetcites [22] Fogarty N.D. Marhaver K.L. Coral spawning, unsynchronized Science. 365 2019 987 988 10.1126/science.aay7457 31488677 source
• Not checked yetcites [23] Shlesinger T. Loya Y. Breakdown in spawning synchrony: a silent threat to coral persistence Science. 365 2019 1002 1007 10.1126/science.aax0110 31488683 source

In the paper

“but those species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies.”

In the paper

“Consistently, many marine species exhibit lunar rhythms, and also the number of documented “lunar-rhythmic” terrestrial species is increasing.”

In the paper

“As external fertilization is frequent among these animals, its synchronization with a reliable environmental cycle maximizes the probability that eggs and sperms encounter, and hence is critical for the survival of these species.”

In the paper

“In animals where the gonads contribute to a large proportion of the body mass, such as sea urchins or mussels, this effect is particularly prominent, leading indeed to significant changes in body mass”

In the paper

“In this case, the spawning occurred 17–18 days after mating, in a precise lunar phase, between LQM and NM [19].”

What the sources say

• Not checked yetcites [19] A.M. Adamczewska, S. Morris, Ecology and behavior of Gecarcoidea natalis, the Christmas Island red crab, during the annual breeding migration, (2001) 305–320. 11441973 source

In the paper

“Moreover, recent high-throughput analyses provide useful leads toward pathways, as well as molecular markers.”

In the paper

“The anomalistic cycle, modulating the proximity of our satellite to earth, can impact for instance on tides amplitude during the synodic month (spring–neap tides cycle, 14.76 days), although slightly out of phase (13.78 days from perigee to apogee) [5,7].”

What the sources say

• Not checked yetcites [5] Coughenour C.L. Archer A.W. Lacovara K.J. Tides, tidalites, and secular changes in the earth–moon system Earth-Science Rev. 97 2009 59 79 10.1016/j.earscirev.2009.09.002 source
• Not checked yetcites [7] Kvale E.P. The origin of neap–spring tidal cycles Mar. Geol. 235 2006 5 18 10.1016/j.margeo.2006.10.001 source

In the paper

“Organisms follow diverse lunar geophysical/astronomical rhythms, which differ significantly in terms of period length: from hours (circalunidian and circatidal rhythms) to days (circasemilunar and circalunar cycles).”

In the paper

“While for short and long lunar period lengths marine examples are very well established, this is less clear for terrestrial organisms.”

In the paper

“Most of the genes analyzed showed similar circadian expression profiles in the two different lunar phases, but significantly higher mRNA levels during FR-FM were found for pdp1, period, clock, and tim (see Figure 2), suggesting that a subset of circadian clock transcripts is affected by the circalunar clock, independently of nocturnal light cues.”

What the sources say

• Not checked yetcites [28] Zantke J. Ishikawa-Fujiwara T. Arboleda E. Lohs C. Schipany K. Hallay N. Straw A.D. Todo T. Circadian and circalunar clock interactions in a marine annelid Cell Rep. 5 2013 99 113 10.1016/j.celrep.2013.08.031 24075994 PMC3913041 source

In the paper

“These data suggest that the integration of multiple environmental features and/or the specific light spectrum of sunlight and moonlight might affect the expression of these genes.”

In the paper

“In spite of the increasing literature, the elucidation of the mechanisms underlying circalunar/circasemilunar and circatidal/circalunidian rhythms is still at an early stage.”

In the paper

“In this species, the circalunar clock seems to also affect locomotor activity levels, with worms showing a weaker circadian rhythmicity during free-running FM (FR-FM) compared to NM.”

What the sources say

• Not checked yetcites [28] Zantke J. Ishikawa-Fujiwara T. Arboleda E. Lohs C. Schipany K. Hallay N. Straw A.D. Todo T. Circadian and circalunar clock interactions in a marine annelid Cell Rep. 5 2013 99 113 10.1016/j.celrep.2013.08.031 24075994 PMC3913041 source

In the paper

“Before this time, the scientific literature is rich in examples of other rhythms, including tidal and monthly. Those were mainly focused on behavioral observations and include many studies that provide evidence for free-running rhythms (for overviews, see [24,25]).”

What the sources say

• Not checked yetcites [24] Fingerman M. Lunar rhythmicity in marine organisms Am. Nat. 91 1957 167 178 source
• Not checked yetcites [25] Numata H. Helm B. Annual, Lunar, and Tidal Clocks: Patterns and Mechanisms of Nature’s Enigmatic Rhythms 2014 Springer

In the paper

“In the reef-building coral Acropora millepora, which reproduces once every year integrating both seasonal, lunar and daily cues, natural FM, as well as artificial night illumination mimicking FM, have been shown to impact on clock genes expression.”

What the sources say

• Not checked yetcites [26] Levy O. Appelbaum L. Leggat W. Gothlif Y. Hayward D.C. Miller D.J. Hoegh-Guldberg O. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora Science. 318 2007 467 470 10.1126/science.1145432 17947585 source

In the paper

“Both cry1 and cry2 were expressed in the ectodermal layer of larvae and adults, and their mRNA levels peaked during daylight phases.”

What the sources say

• Not checked yetcites [26] Levy O. Appelbaum L. Leggat W. Gothlif Y. Hayward D.C. Miller D.J. Hoegh-Guldberg O. Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora Science. 318 2007 467 470 10.1126/science.1145432 17947585 source

In the paper

“For instance, only cry1 (but not cry2) was affected by exposure to DD, whereas, although not significantly, cry2 increased under natural moonlight compared to the artificial one during both LQM and FM [27,31].”

What the sources say

• Not checked yetcites [27] Brady A.K. Willis B.L. Harder L.D. Vize P.D. Lunar phase modulates circadian gene expression cycles in the broadcast spawning coral Acropora millepora Biol. Bull. 230 2016 130 142 10.1086/BBLv230n2p130 27132135 source
• Not checked yetcites [31] Brady A.K. Snyder K.A. Vize P.D. Circadian cycles of gene expression in the coral, Acropora millepora PLoS One 6 2011 10.1371/journal.pone.0025072 PMC3176305 21949855 source

In the paper

“This phenomenon threatens several species, not only corals, but entire reef communities.”

In the paper

“These and other data reported in this review suggest a high level of data variability, likely due to differences in experimental regimes, as well as strong environmental and possibly population variability.”

In the paper

“This intertidal isopod showed robust tidal rhythmicity after being caught in the wild and released in DD, suggesting the existence of a true circatidal endogenous oscillator.”

What the sources say

• Not checked yetcites [10] Zhang L. Hastings M.H. Green E.W. Tauber E. Sladek M. Webster S.G. Kyriacou C.P. Wilcockson D.C. Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra Curr. Biol. 23 2013 1863 1873 10.1016/j.cub.2013.08.038 24076244 PMC3793863 source

In the paper

“Furthermore, circadian rhythm disruption through LL exposure affected neither the tidal swimming period nor overall activity levels [10].”

What the sources say

• Not checked yetcites [10] Zhang L. Hastings M.H. Green E.W. Tauber E. Sladek M. Webster S.G. Kyriacou C.P. Wilcockson D.C. Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra Curr. Biol. 23 2013 1863 1873 10.1016/j.cub.2013.08.038 24076244 PMC3793863 source

In the paper

“Circatidal clocks and their relation with circadian clocks are particularly interesting, because in essence a 12.4 h period is just half of 24.8 h, i.e. a period covered by the conventional core circadian clock network.”

In the paper

“Genetic linkage analysis identified two specific chromosomal regions responsible for diurnal emergence and two related to lunar timing.”

What the sources say

• Not checked yetcites [46] Kaiser T.S. Poehn B. Szkiba D. Preussner M. Sedlazeck F.J. Zrim A. Neumann T. Nguyen L.T. The genomic basis of circadian and circalunar timing adaptations in a midge Nature. 540 2016 69 73 10.1038/nature20151 27871090 PMC5133387 source

In the paper

“Thus, the data presented might actually suggest the presence of both a photo-repressive mechanism and an endogenous clock contributing together to the circalunar timing.”

In the paper

“In spite of the observed phase delay, the amplitude of tidal oscillations was robust and comparable to the untreated control.”

What the sources say

• Not checked yetcites [10] Zhang L. Hastings M.H. Green E.W. Tauber E. Sladek M. Webster S.G. Kyriacou C.P. Wilcockson D.C. Dissociation of circadian and circatidal timekeeping in the marine crustacean Eurydice pulchra Curr. Biol. 23 2013 1863 1873 10.1016/j.cub.2013.08.038 24076244 PMC3793863 source

In the paper

“Moreover, per4 showed a robust oscillation over the lunar cycle under all the light regimes, but in antiphase compared to cry3.”

What the sources say

• Not checked yetcites [50] Toda R. Okano K. Takeuchi Y. Yamauchi C. Fukushiro M. Takemura A. Okano T. Hypothalamic expression and moonlight-independent changes of Cry3 and Per4 implicate their roles in lunar clock oscillators of the lunar-responsive goldlined spinefoot PLoS One 9 2014 10.1371/journal.pone.0109119 PMC4182804 25272159 source

In the paper

“These data potentially indicate the existence of a circatidal clock in the grass puffer brain, which, together with the circadian clock, might contribute to set the proper daily and lunar-related reproductive rhythms.”

In the paper

“Thus, the authors suggested that peaks of PRX activity and mitochondrially encoded transcript levels might anticipate changes in the energy demand and reactive oxygen species production originating from the prevailing metabolic program, following in this case a circatidal rest/activity rhythm.”

What the sources say

• Not checked yetcites [54] O’Neill J.S. Lee K.D. Zhang L. Feeney K. Webster S.G. Blades M.J. Kyriacou C.P. Hastings M.H. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra Curr. Biol. 25 2015 R326 R327 10.1016/j.cub.2015.02.052 25898100 PMC4406942 source

In the paper

“Moreover, melatonin synthesis is exquisitely light sensitive, inhibited by light exposure, and fueled in the dark [48,58,59]”

What the sources say

• Not checked yetcites [48] Takemura A. Susilo E.S. Rahman M.D.S. Morita M. Perception and possible utilization of moonlight intensity for reproductive activities in a lunar-synchronized spawner, the golden rabbitfish J. Exp. Zool. Part A Comp. Exp. Biol. 301 2004 844 851 10.1002/jez.a.105 15449345 source
• Not checked yetcites [58] Rahman M.S. Kim B.H. Takemura A. Park C.B. Lee Y.D. Effects of moonlight exposure on plasma melatonin rhythms in the seagrass rabbitfish, Siganus canaliculatus J. Biol. Rhythm. 19 2004 325 334 10.1177/0748730404266712 15245651 source
• Not checked yetcites [59] Rahman M.S. Kim B.H. Takemura A. Park C.B. Lee Y.D. Influence of light-dark and lunar cycles on the ocular melatonin rhythms in the seagrass rabbitfish, a lunar-synchronized spawner J. Pineal Res. 37 2004 122 128 10.1111/j.1600-079X.2004.00147.x 15298671 source

In the paper

“Given its role as an endocrine mediator of other light-dependent rhythms (daily/circadian, i.e. daily sleep–wake cycle) in vertebrates, also melatonin has been suggested as a potential component of the molecular mechanisms contributing to lunar-regulated rhythms.”

In the paper

“The period of these oscillations was consistent with swimming activity and respiratory rate tidal cycles, which peak around high tides [54,56].”

What the sources say

• Not checked yetcites [54] O’Neill J.S. Lee K.D. Zhang L. Feeney K. Webster S.G. Blades M.J. Kyriacou C.P. Hastings M.H. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra Curr. Biol. 25 2015 R326 R327 10.1016/j.cub.2015.02.052 25898100 PMC4406942 source
• Not checked yetcites [56] Hastings M.H. Semi-lunar variations of endogenous circa-tidal rhythms of activity and respiration in the isopod Eurydice pulchra Mar. Ecol Prog Ser. 4 1981 85 90 10.3354/meps004085 source

In the paper

“Taking all above findings together might start to indicate that the circadian clockwork could be more plastic than previously thought and capable to adjust to the environmental cycle(s) most relevant for a given species [53,54,57].”

What the sources say

• Not checked yetcites [53] Tran D. Perrigault M. Ciret P. Payton L. Bivalve mollusc circadian clock genes can run at tidal frequency Proc. Biol. Sci. 287 2020 20192440 10.1098/rspb.2019.2440 31910786 PMC7003461
• Not checked yetcites [54] O’Neill J.S. Lee K.D. Zhang L. Feeney K. Webster S.G. Blades M.J. Kyriacou C.P. Hastings M.H. Metabolic molecular markers of the tidal clock in the marine crustacean Eurydice pulchra Curr. Biol. 25 2015 R326 R327 10.1016/j.cub.2015.02.052 25898100 PMC4406942 source
• Not checked yetcites [57] Schnytzer Y. Simon-Blecher N. Li J. Ben-Asher H.W. Salmon-Divon M. Achituv Y. Hughes M.E. Levy O. Tidal and diel orchestration of behaviour and gene expression in an intertidal mollusc Sci. Rep. 8 2018 1 13 10.1038/s41598-018-23167-y 29559663 PMC5861051 source

In the paper

“This lack of both circatidal and circadian rhythmicity in clock gene expression is also conceivable with the idea that specific subsets of the core circadian clock might be differentially recruited in a tissue-dependent manner, and depending on cellular context form circadian, circatidal, or circalunidian clocks.”

In the paper

“Laboratory studies provide a better control of the multitude of environmental variables present in nature, allowing the investigation of the single contributions of a certain cue”

In the paper

“the generation of knockouts and transgenic animals clearly allow for a detailed functional dissection that is difficult to meet with other methods”

In the paper

“complex chronobiological changes likely caused by anthropogenic impacts (i.e. light pollution, temperature changes, architectural barriers) that are endangering the world's ecosystems as we know them [22,23], and possibly human health”

What the sources say

• Not checked yetcites [22] Fogarty N.D. Marhaver K.L. Coral spawning, unsynchronized Science. 365 2019 987 988 10.1126/science.aay7457 31488677 source
• Not checked yetcites [23] Shlesinger T. Loya Y. Breakdown in spawning synchrony: a silent threat to coral persistence Science. 365 2019 1002 1007 10.1126/science.aax0110 31488683 source